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Developmental decrease of entorhinal-hippocampal communication in immune-challenged DISC1 knockdown mice

Author

Listed:
  • Xiaxia Xu

    (Center for Molecular Neurobiology, University Medical Center Hamburg-Eppendorf)

  • Lingzhen Song

    (Center for Molecular Neurobiology, University Medical Center Hamburg-Eppendorf)

  • Rebecca Kringel

    (Center for Molecular Neurobiology, University Medical Center Hamburg-Eppendorf)

  • Ileana L. Hanganu-Opatz

    (Center for Molecular Neurobiology, University Medical Center Hamburg-Eppendorf)

Abstract

The prefrontal-hippocampal dysfunction that underlies cognitive deficits in mental disorders emerges during early development. The lateral entorhinal cortex (LEC) is tightly interconnected with both prefrontal cortex (PFC) and hippocampus (HP), yet its contribution to the early dysfunction is fully unknown. Here we show that mice that mimic the dual genetic (G) -environmental (E) etiology (GE mice) of psychiatric risk have poor LEC-dependent recognition memory at pre-juvenile age and abnormal communication within LEC-HP-PFC networks throughout development. These functional and behavioral deficits relate to sparser projections from LEC to CA1 and decreased efficiency of axonal terminals to activate the hippocampal circuits in neonatal GE mice. In contrast, the direct entorhinal drive to PFC is not affected, yet the PFC is indirectly compromised, as target of the under-activated HP. Thus, the entorhinal-hippocampal circuit is already impaired from neonatal age on in GE mice.

Suggested Citation

  • Xiaxia Xu & Lingzhen Song & Rebecca Kringel & Ileana L. Hanganu-Opatz, 2021. "Developmental decrease of entorhinal-hippocampal communication in immune-challenged DISC1 knockdown mice," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27114-w
    DOI: 10.1038/s41467-021-27114-w
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    References listed on IDEAS

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    1. Jim van Os & Gunter Kenis & Bart P. F. Rutten, 2010. "The environment and schizophrenia," Nature, Nature, vol. 468(7321), pages 203-212, November.
    2. Kei M. Igarashi & Li Lu & Laura L. Colgin & May-Britt Moser & Edvard I. Moser, 2014. "Coordination of entorhinal–hippocampal ensemble activity during associative learning," Nature, Nature, vol. 510(7503), pages 143-147, June.
    3. Andreas Meyer-Lindenberg, 2010. "From maps to mechanisms through neuroimaging of schizophrenia," Nature, Nature, vol. 468(7321), pages 194-202, November.
    4. Albert Tsao & Jørgen Sugar & Li Lu & Cheng Wang & James J. Knierim & May-Britt Moser & Edvard I. Moser, 2018. "Integrating time from experience in the lateral entorhinal cortex," Nature, Nature, vol. 561(7721), pages 57-62, September.
    5. Thomas R. Insel, 2010. "Rethinking schizophrenia," Nature, Nature, vol. 468(7321), pages 187-193, November.
    6. Bernhard P. Staresina & Thomas P. Reber & Johannes Niediek & Jan Boström & Christian E. Elger & Florian Mormann, 2019. "Recollection in the human hippocampal-entorhinal cell circuitry," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    7. Rustem Khazipov & Anton Sirota & Xavier Leinekugel & Gregory L. Holmes & Yehezkel Ben-Ari & György Buzsáki, 2004. "Early motor activity drives spindle bursts in the developing somatosensory cortex," Nature, Nature, vol. 432(7018), pages 758-761, December.
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